Professor Peter Hedden graduated with BSc (1969) and PhD (1973) degrees in chemistry from the University of Bristol. After post-doctoral positions at the University of Göttingen, Germany, with Jan Graebe and at UCLA, USA, with Bernard Phinney, he joined East Malling Research Station, in Kent, United Kingdom in 1981. He moved to Long Ashton Research Station (LARS), Bristol, UK, in 1984 and then to Rothamsted Research after the closure of LARS in 2003. His main research interest throughout his career has been the biosynthesis of the gibberellin plant hormones, working initially on delineating the biosynthetic pathways, then on the isolation and characterization of the biosynthetic enzymes and latterly on their regulation by developmental and environmental factors. Current research includes exploiting the gibberellin biosynthesis and signal transduction pathways for the introduction of desirable traits into crop species.Dr Steve Thomas graduated BSc from the University of Southampton in 1991. He gained a PhD in biochemistry at Bristol University in 1996. In the same year he started postdoctoral work at Long Ashton Research Station where he spent four years investigating the regulation of gibberellin biosynthesis and inactivation in sugar beet and Arabidopsis. He then spent three and a half years in Tai-ping Sun’s Laboratory at Duke University dissecting the signalling pathways controlling gibberellin-mediated degradation of DELLA proteins in Arabidopsis. In 2004, he returned to the UK to work with Dr Andy Phillips and Prof. Peter Hedden in the Hormone Signalling Group at Rothamsted Research as a Senior Scientist. He is currently a member of the 20:20 Wheat® Institute Strategic Programme at Rothamsted Research, with his research  focused on improving grain yields in wheat by manipulating plant hormone signalling.

• List of Contributors xvPreface xvii1 Signal Achievements in Gibberellin Research: The Second Half-Century 1Valerie M. Sponsel1.1 Introduction 11.2 Gibberellin biosynthesis 61.3 Gibberellin signalling 171.4 Physiological responses to gibberellins 25References 292 Gibberellin Biosynthesis in Higher Plants 37Peter Hedden2.1 Introduction 372.2 Synthesis of ent-kaurene 392.2.1 Formation of trans-geranylgeranyl diphosphate 392.2.2 Formation of ent-kaurene from trans-geranylgeranyl diphosphate 402.3 Reactions catalysed by cytochrome P450 mono-oxygenases 422.4 Reactions catalysed by 2-oxoglutarate-dependent dioxygenases 452.5 Sites of gibberellin biosynthesis 492.6 Regulation of gibberellin biosynthesis 502.6.1 Developmental control 502.6.2 Gibberellin homoeostasis 512.6.3 Regulation by other hormones 542.6.4 Regulation by environmental factors 552.7 Concluding remarks 59Acknowledgements 60References 603 Inactivation Processes 73Hiroshi Magome and Yuji Kamiya3.1 Introduction 733.2 Gibberellin inactivation 753.2.1 Gibberellin 2-oxidase 753.2.2 Gibberellin methyltransferase 773.2.3 Gibberellin 16,17-oxidase 783.2.4 Gibberellin 13-oxidase and 12α-oxidase 783.2.5 Conjugation with sugar 803.3 Regulation of gibberellin inactivation 803.3.1 Developmental regulation 813.3.2 Gibberellin homoeostasis 823.3.3 Regulation by other hormones 833.3.4 Environmental regulation 843.4 Concluding remarks 87References 884 Gibberellin Transport 95Jonathan Dayan4.1 Introduction 954.2 Gibberellins can be translocated along plant bodies 964.3 Gibberellin transport in seeds 1004.4 Pattern of gibberellin biosynthesis in transport analysis 1014.5 Grafting experiments 1034.6 Significance for secondary growth 1044.7 Orientation of gibberellin signal flow: source and sink tissues 1074.8 Monitoring intra- and intercellular gibberellin concentration 1104.9 Conclusion: new aspects for gibberellin transport 1114.9.1 Potential transporters 1114.9.2 Analysis through perception 1124.9.3 Links to sugar transport 112Acknowledgements 113References 1145 Gibberellins in Fungi, Bacteria and Lower Plants: Biosynthesis, Function and Evolution 121Bettina Tudzynski, Lena Studt and María Cecilia Rojas5.1 Introduction 1225.2 Gibberellin biosynthesis in fungi 1225.2.1 The biosynthetic pathway in F. fujikuroi: genes and enzymes 1225.2.2 Gibberellin production in distantly related fungi 1265.2.3 Evolution of the gibberellin biosynthetic gene cluster in fungi 1285.2.4 The role of gibberellins in plant infection 1315.2.5 Strain improvement 1325.3 Gibberellin biosynthesis in bacteria 1335.3.1 Free-living rhizobacteria 1335.3.2 Symbiotic rhizobacteria: genes and reactions of the gibberellin biosynthetic pathway 1345.3.3 Function and evolution 1375.4 Gibberellin biosynthesis and signalling components in lower plants 1395.5 Concluding remarks 143References 1446 Gibberellin Hormone Signal Perception: Down-Regulating DELLA Repressors of Plant Growth and Development 153Sven K. Nelson and Camille M. Steber6.1 Introduction 1546.2 DELLA proteins are repressors of gibberellin responses 1546.3 Gibberellin signalling lifts DELLA repression of gibberellin responses 1576.4 The gibberellin receptor GID1 (GA-INSENSITIVE DWARF1) 1596.5 The structural requirements for gibberellin binding by GID1 1616.6 The structural requirements for the GID1-DELLA protein–protein interaction 1626.7 The DELLA destruction model: negative regulation of DELLA repressors by SLY1/GID2 and the ubiquitin-proteasome pathway 1666.8 Regulation of DELLA by phosphorylation and O-GlcNAc modification 1696.9 Evidence for gibberellin-independent DELLA regulation 1736.10 Evidence for gibberellin signalling without DELLA destruction 1756.11 Concluding remarks 177Acknowledgements 179References 1797 DELLA Proteins: Master Regulators of Gibberellin-Responsive Growth and Development 189Stephen G. Thomas, Miguel A. Blázquez and David Alabadí7.1 Introduction 1907.2 DELLAs regulate downstream gibberellin signalling 1917.3 Gibberellins relieve DELLA-growth repression by targeting their degradation 1937.4 Functional diversification of DELLA genes 1947.5 DELLA activity invokes rapid changes in the transcriptome 1977.6 DELLA proteins activate transcription 1987.7 DELLAs regulate transcription by physical interaction with transcriptional regulators 1997.7.1 DELLAs sequester bona fide TFs by physical interaction 2007.7.2 DELLAs interact with TFs in the context of promoters 2047.7.3 DELLAs interact with other transcriptional regulators 2067.7.4 DELLAs regulate chromatin dynamics 2087.8 A non-genomic response regulated by DELLAs 2097.9 Analysis of DELLA protein structure-function 2107.10 GAMYB: A transcriptional regulator of gibberellin responses during cereal grain germination and pollen development 2137.10.1 GAMYB positively regulates gene expression in cereal aleurone cells 2147.10.2 GAMYB regulates gibberellin-dependent anther development 2167.11 Concluding remarks 217Acknowledgements 218References 2188 Interactions Between Gibberellins and other Hormones 229John J. Ross, Asemeh Miraghazadeh, Amelia H. Beckett, Laura J. Quittenden and Erin L. McAdam8.1 Introduction 2298.2 Interactions involving effects of other hormones on gibberellin levels 2308.2.1 Auxin promotes gibberellin biosynthesis 2308.2.2 Ethylene inhibits gibberellin biosynthesis 2318.2.3 Do gibberellin and abscisic acid inhibit each other’s synthesis? 2328.2.4 Do brassinosteroids act by affecting gibberellin levels? 2348.2.5 Possible effects of other hormones on gibberellin synthesis 2348.3 Interactions between hormone signal transduction pathways 2348.3.1 Do other hormones affect DELLA stability? 2358.3.2 DELLAs interact with proteins from the signaling pathways of other hormones 2378.4 Gibberellins and auxin transport 2458.5 Conclusion 246Acknowledgements 247References 2479 Gibberellins and Seed Germination 253Terezie Urbanova and Gerhard Leubner-Metzger9.1 Introduction 2549.2 Spatiotemporal expression of gibberellin metabolism during Brassicaceae seed germination 2549.3 Gibberellin signalling and seed germination 2649.3.1 The GID1ac and GID1b pathways in seeds 2649.3.2 DELLA proteins and seed germination 2689.4 Gibberellin and abiotic stress factors: thermoinhibition of seed germination 2709.5 Gibberellin and biotic stress factors: allelochemical interference of gibberellin biosynthesis during seed germination 2739.6 Conclusions and perspectives 276Acknowledgements 277References 27710 Gibberellins and Plant Vegetative Growth 285Cristina Martínez, Ana Espinosa-Ruiz and Salomé Prat10.1 Introduction 28510.2 Gibberellins and shoot development 28810.2.1 Control of SAM function and leaf size 28910.2.2 Elongation of the hypocotyl 29010.2.3 Apical hook formation 29510.3 Gibberellin function in root development 29810.3.1 Hormonal control of root growth 29810.3.2 Gibberellin signalling from the endodermis 30210.3.3 DELLAs downstream signalling in the root 30410.3.4 DELLAs promote mycorrhizal symbiosis 30610.4 Growth under unfavourable conditions 30810.4.1 DELLAs promote resistance to abiotic stress 30810.4.2 DELLAs and biotic stress 31010.5 Concluding remarks 311References 31211 Gibberellins and Plant Reproduction 323Andrew R.G. Plackett and Zoe A. Wilson11.1 Introduction 32311.2 The floral transition 32411.2.1 Gibberellin promotes flowering through multiple interacting pathways 32411.2.2 Sites of gibberellin biosynthesis and action during the floral transition 32911.2.3 Gibberellin and flowering in perennial species 33111.3 Floral development 33111.3.1 Floral patterning and early development 33211.3.2 Gibberellin and fertility 33411.4 Seed and fruit development 34011.4.1 Fruit development 34111.4.2 Embryo and seed development 345Acknowledgements 348References 34812 Chemical Regulators of Gibberellin Status and their Application in Plant Production 359Wilhelm Rademacher12.1 Introduction 35912.2 Gibberellins 36112.3 Inhibitors of gibberellin biosynthesis 36312.3.1 Quaternary ammonium compounds 36512.3.2 Compounds with a nitrogen-containing heterocycle 36612.3.3 Structural mimics of 2-oxoglutaric acid 36912.3.4 16,17-Dihydro-gibberellins 37112.4 Uses for gibberellins and inhibitors of gibberellin biosynthesis in crop production 37212.4.1 Wheat, barley, rye, oats and other small-grain cereals 37312.4.2 Rice 37612.4.3 Sugarcane 37712.4.4 Pasture and turf grasses 37712.4.5 Oilseed rape 37912.4.6 Cotton 37912.4.7 Peanuts 38112.4.8 Opium poppy 38212.4.9 Fruit trees growing in temperate climate 38212.4.10 Fruit and nut trees growing in subtropical and tropical climates 38512.4.11 Grapevines 38712.4.12 Ornamentals 38912.4.13 Hybrid seed production 39112.5 Outlook 391References 39113 Genetic Control of Gibberellin Metabolism and Signalling in Crop Improvement 405Andrew L. Phillips13.1 Introduction 40513.2 The REDUCED HEIGHT-1 (Rht-1) alleles of wheat 40613.2.1 Pleiotropic effects of Rht-1 alleles 41013.2.2 Rht-1 orthologues in other crop species 41213.3 The SEMI-DWARF-1(SD-1) alleles of rice 41313.4 The ELONGATED UPPERMOST INTERNODE (EUI) gene of rice 41513.5 Commercially useful alleles of other genes from the gibberellin pathway 41613.6 Transgenic approaches to manipulation of gibberellin-dependent processes in crops 41913.6.1 Cereals 41913.6.2 Other crop species 42013.7 Conclusions 423Acknowledgements 424References 424Appendix The structures of the gibberellins 431Index 437

Professor Peter Hedden graduated with BSc (1969) and PhD (1973) degrees in chemistry from the University of Bristol. After post-doctoral positions at the University of Göttingen, Germany, with Jan Graebe and at UCLA, USA, with Bernard Phinney, he joined East Malling Research Station, in Kent, United Kingdom in 1981. He moved to Long Ashton Research Station (LARS), Bristol, UK, in 1984 and then to Rothamsted Research after the closure of LARS in 2003. His main research interest throughout his career has been the biosynthesis of the gibberellin plant hormones, working initially on delineating the biosynthetic pathways, then on the isolation and characterization of the biosynthetic enzymes and latterly on their regulation by developmental and environmental factors. Current research includes exploiting the gibberellin biosynthesis and signal transduction pathways for the introduction of desirable traits into crop species.Dr Steve Thomas graduated BSc from the University of Southampton in 1991. He gained a PhD in biochemistry at Bristol University in 1996. In the same year he started postdoctoral work at Long Ashton Research Station where he spent four years investigating the regulation of gibberellin biosynthesis and inactivation in sugar beet and Arabidopsis. He then spent three and a half years in Tai-ping Sun’s Laboratory at Duke University dissecting the signalling pathways controlling gibberellin-mediated degradation of DELLA proteins in Arabidopsis. In 2004, he returned to the UK to work with Dr Andy Phillips and Prof. Peter Hedden in the Hormone Signalling Group at Rothamsted Research as a Senior Scientist. He is currently a member of the 20:20 Wheat® Institute Strategic Programme at Rothamsted Research, with his research  focused on improving grain yields in wheat by manipulating plant hormone signalling.

• List of Contributors xvPreface xvii1 Signal Achievements in Gibberellin Research: The Second Half-Century 1Valerie M. Sponsel1.1 Introduction 11.2 Gibberellin biosynthesis 61.3 Gibberellin signalling 171.4 Physiological responses to gibberellins 25References 292 Gibberellin Biosynthesis in Higher Plants 37Peter Hedden2.1 Introduction 372.2 Synthesis of ent-kaurene 392.2.1 Formation of trans-geranylgeranyl diphosphate 392.2.2 Formation of ent-kaurene from trans-geranylgeranyl diphosphate 402.3 Reactions catalysed by cytochrome P450 mono-oxygenases 422.4 Reactions catalysed by 2-oxoglutarate-dependent dioxygenases 452.5 Sites of gibberellin biosynthesis 492.6 Regulation of gibberellin biosynthesis 502.6.1 Developmental control 502.6.2 Gibberellin homoeostasis 512.6.3 Regulation by other hormones 542.6.4 Regulation by environmental factors 552.7 Concluding remarks 59Acknowledgements 60References 603 Inactivation Processes 73Hiroshi Magome and Yuji Kamiya3.1 Introduction 733.2 Gibberellin inactivation 753.2.1 Gibberellin 2-oxidase 753.2.2 Gibberellin methyltransferase 773.2.3 Gibberellin 16,17-oxidase 783.2.4 Gibberellin 13-oxidase and 12α-oxidase 783.2.5 Conjugation with sugar 803.3 Regulation of gibberellin inactivation 803.3.1 Developmental regulation 813.3.2 Gibberellin homoeostasis 823.3.3 Regulation by other hormones 833.3.4 Environmental regulation 843.4 Concluding remarks 87References 884 Gibberellin Transport 95Jonathan Dayan4.1 Introduction 954.2 Gibberellins can be translocated along plant bodies 964.3 Gibberellin transport in seeds 1004.4 Pattern of gibberellin biosynthesis in transport analysis 1014.5 Grafting experiments 1034.6 Significance for secondary growth 1044.7 Orientation of gibberellin signal flow: source and sink tissues 1074.8 Monitoring intra- and intercellular gibberellin concentration 1104.9 Conclusion: new aspects for gibberellin transport 1114.9.1 Potential transporters 1114.9.2 Analysis through perception 1124.9.3 Links to sugar transport 112Acknowledgements 113References 1145 Gibberellins in Fungi, Bacteria and Lower Plants: Biosynthesis, Function and Evolution 121Bettina Tudzynski, Lena Studt and María Cecilia Rojas5.1 Introduction 1225.2 Gibberellin biosynthesis in fungi 1225.2.1 The biosynthetic pathway in F. fujikuroi: genes and enzymes 1225.2.2 Gibberellin production in distantly related fungi 1265.2.3 Evolution of the gibberellin biosynthetic gene cluster in fungi 1285.2.4 The role of gibberellins in plant infection 1315.2.5 Strain improvement 1325.3 Gibberellin biosynthesis in bacteria 1335.3.1 Free-living rhizobacteria 1335.3.2 Symbiotic rhizobacteria: genes and reactions of the gibberellin biosynthetic pathway 1345.3.3 Function and evolution 1375.4 Gibberellin biosynthesis and signalling components in lower plants 1395.5 Concluding remarks 143References 1446 Gibberellin Hormone Signal Perception: Down-Regulating DELLA Repressors of Plant Growth and Development 153Sven K. Nelson and Camille M. Steber6.1 Introduction 1546.2 DELLA proteins are repressors of gibberellin responses 1546.3 Gibberellin signalling lifts DELLA repression of gibberellin responses 1576.4 The gibberellin receptor GID1 (GA-INSENSITIVE DWARF1) 1596.5 The structural requirements for gibberellin binding by GID1 1616.6 The structural requirements for the GID1-DELLA protein–protein interaction 1626.7 The DELLA destruction model: negative regulation of DELLA repressors by SLY1/GID2 and the ubiquitin-proteasome pathway 1666.8 Regulation of DELLA by phosphorylation and O-GlcNAc modification 1696.9 Evidence for gibberellin-independent DELLA regulation 1736.10 Evidence for gibberellin signalling without DELLA destruction 1756.11 Concluding remarks 177Acknowledgements 179References 1797 DELLA Proteins: Master Regulators of Gibberellin-Responsive Growth and Development 189Stephen G. Thomas, Miguel A. Blázquez and David Alabadí7.1 Introduction 1907.2 DELLAs regulate downstream gibberellin signalling 1917.3 Gibberellins relieve DELLA-growth repression by targeting their degradation 1937.4 Functional diversification of DELLA genes 1947.5 DELLA activity invokes rapid changes in the transcriptome 1977.6 DELLA proteins activate transcription 1987.7 DELLAs regulate transcription by physical interaction with transcriptional regulators 1997.7.1 DELLAs sequester bona fide TFs by physical interaction 2007.7.2 DELLAs interact with TFs in the context of promoters 2047.7.3 DELLAs interact with other transcriptional regulators 2067.7.4 DELLAs regulate chromatin dynamics 2087.8 A non-genomic response regulated by DELLAs 2097.9 Analysis of DELLA protein structure-function 2107.10 GAMYB: A transcriptional regulator of gibberellin responses during cereal grain germination and pollen development 2137.10.1 GAMYB positively regulates gene expression in cereal aleurone cells 2147.10.2 GAMYB regulates gibberellin-dependent anther development 2167.11 Concluding remarks 217Acknowledgements 218References 2188 Interactions Between Gibberellins and other Hormones 229John J. Ross, Asemeh Miraghazadeh, Amelia H. Beckett, Laura J. Quittenden and Erin L. McAdam8.1 Introduction 2298.2 Interactions involving effects of other hormones on gibberellin levels 2308.2.1 Auxin promotes gibberellin biosynthesis 2308.2.2 Ethylene inhibits gibberellin biosynthesis 2318.2.3 Do gibberellin and abscisic acid inhibit each other’s synthesis? 2328.2.4 Do brassinosteroids act by affecting gibberellin levels? 2348.2.5 Possible effects of other hormones on gibberellin synthesis 2348.3 Interactions between hormone signal transduction pathways 2348.3.1 Do other hormones affect DELLA stability? 2358.3.2 DELLAs interact with proteins from the signaling pathways of other hormones 2378.4 Gibberellins and auxin transport 2458.5 Conclusion 246Acknowledgements 247References 2479 Gibberellins and Seed Germination 253Terezie Urbanova and Gerhard Leubner-Metzger9.1 Introduction 2549.2 Spatiotemporal expression of gibberellin metabolism during Brassicaceae seed germination 2549.3 Gibberellin signalling and seed germination 2649.3.1 The GID1ac and GID1b pathways in seeds 2649.3.2 DELLA proteins and seed germination 2689.4 Gibberellin and abiotic stress factors: thermoinhibition of seed germination 2709.5 Gibberellin and biotic stress factors: allelochemical interference of gibberellin biosynthesis during seed germination 2739.6 Conclusions and perspectives 276Acknowledgements 277References 27710 Gibberellins and Plant Vegetative Growth 285Cristina Martínez, Ana Espinosa-Ruiz and Salomé Prat10.1 Introduction 28510.2 Gibberellins and shoot development 28810.2.1 Control of SAM function and leaf size 28910.2.2 Elongation of the hypocotyl 29010.2.3 Apical hook formation 29510.3 Gibberellin function in root development 29810.3.1 Hormonal control of root growth 29810.3.2 Gibberellin signalling from the endodermis 30210.3.3 DELLAs downstream signalling in the root 30410.3.4 DELLAs promote mycorrhizal symbiosis 30610.4 Growth under unfavourable conditions 30810.4.1 DELLAs promote resistance to abiotic stress 30810.4.2 DELLAs and biotic stress 31010.5 Concluding remarks 311References 31211 Gibberellins and Plant Reproduction 323Andrew R.G. Plackett and Zoe A. Wilson11.1 Introduction 32311.2 The floral transition 32411.2.1 Gibberellin promotes flowering through multiple interacting pathways 32411.2.2 Sites of gibberellin biosynthesis and action during the floral transition 32911.2.3 Gibberellin and flowering in perennial species 33111.3 Floral development 33111.3.1 Floral patterning and early development 33211.3.2 Gibberellin and fertility 33411.4 Seed and fruit development 34011.4.1 Fruit development 34111.4.2 Embryo and seed development 345Acknowledgements 348References 34812 Chemical Regulators of Gibberellin Status and their Application in Plant Production 359Wilhelm Rademacher12.1 Introduction 35912.2 Gibberellins 36112.3 Inhibitors of gibberellin biosynthesis 36312.3.1 Quaternary ammonium compounds 36512.3.2 Compounds with a nitrogen-containing heterocycle 36612.3.3 Structural mimics of 2-oxoglutaric acid 36912.3.4 16,17-Dihydro-gibberellins 37112.4 Uses for gibberellins and inhibitors of gibberellin biosynthesis in crop production 37212.4.1 Wheat, barley, rye, oats and other small-grain cereals 37312.4.2 Rice 37612.4.3 Sugarcane 37712.4.4 Pasture and turf grasses 37712.4.5 Oilseed rape 37912.4.6 Cotton 37912.4.7 Peanuts 38112.4.8 Opium poppy 38212.4.9 Fruit trees growing in temperate climate 38212.4.10 Fruit and nut trees growing in subtropical and tropical climates 38512.4.11 Grapevines 38712.4.12 Ornamentals 38912.4.13 Hybrid seed production 39112.5 Outlook 391References 39113 Genetic Control of Gibberellin Metabolism and Signalling in Crop Improvement 405Andrew L. Phillips13.1 Introduction 40513.2 The REDUCED HEIGHT-1 (Rht-1) alleles of wheat 40613.2.1 Pleiotropic effects of Rht-1 alleles 41013.2.2 Rht-1 orthologues in other crop species 41213.3 The SEMI-DWARF-1(SD-1) alleles of rice 41313.4 The ELONGATED UPPERMOST INTERNODE (EUI) gene of rice 41513.5 Commercially useful alleles of other genes from the gibberellin pathway 41613.6 Transgenic approaches to manipulation of gibberellin-dependent processes in crops 41913.6.1 Cereals 41913.6.2 Other crop species 42013.7 Conclusions 423Acknowledgements 424References 424Appendix The structures of the gibberellins 431Index 437